The human mycobiome in health and disease

Genome Medicine

Volumn 5, Issue 7, 2013, Pages

  Cui, Lijia ^a   Morris, Alison ^a   Ghedin, Elodie ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERNAL TRANSCRIBED SPACER; RIBOSOME DNA;

ACQUIRED IMMUNE DEFICIENCY SYNDROME; ACREMONIUM; ALLERGY; ALTERNARIA; AMPLICON; ANTIFUNGAL RESISTANCE; ASCOMYCETES; ASPERGILLUS; ASPERGILLUS FUMIGATUS; ASYMPTOMATIC INFECTION; ATOPIC DERMATITIS; BASIDIOMYCETES; BLASTOMYCES; CANDIDA; CANDIDA ALBICANS; CANDIDA DUBLINIENSIS; CANDIDA GLABRATA; CLADOSPORIUM; COCCIDIOIDES; CROHN DISEASE; CRYPTOCOCCUS NEOFORMANS; CYSTIC FIBROSIS; DISEASE COURSE; ENDOSCOPIC BIOPSY; FUNGUS; FUNGUS CULTURE; GEL ELECTROPHORESIS; GEOTRICHUM; GRAFT VERSUS HOST REACTION; HEALTH STATUS; HEPATITIS B; HISTOPLASMA; HOST PATHOGEN INTERACTION; HUMAN; HYPHOMYCETES; IN SITU HYBRIDIZATION; LIVER CIRRHOSIS; MALASSEZIA; MICROBIAL DIVERSITY; MICROBIOME; MICROSPORUM; MYCOBACTERIUM; MYCOBIOME; MYCOSIS; NONHUMAN; PATHOGENESIS; PENICILLIUM; PNEUMOCYSTIS; PRIORITY JOURNAL; PSEUDOMONAS; PSEUDOMONAS AERUGINOSA; PSORIASIS; PYROSEQUENCING; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; REVIEW; RHODOTORULA; RNA GENE; SACCHAROMYCES BOULARDII; SINGLE NUCLEOTIDE POLYMORPHISM; SPUTUM ANALYSIS; SUPERINFECTION; TRICHOPHYTON; TRICHOSPORON;

EID: 84880335170     PISSN: None     EISSN: 1756994X     Source Type: Journal    
DOI: 10.1186/gm467     Document Type: Review

References (76)

1. Hassall A. On the development of Torulæ in the urine, and on the relation of these fungi to albuminous and saccharine urine. Med Chir Trans 1853, 36:23-78. 2104146, 20896006.
2. Chiene J, Ewart JC. Do bacteria or their germs exist in the organs of healthy living animals?. J Anat Physiol 1878, 12:448-453. 1309796, 17231209.
3. Relman DA. New technologies, human-microbe interactions, and the search for previously unrecognized pathogens. J Infect Dis 2002, 186:S254-S258. 10.1086/344935, 12424706.
4. Mitreva M. Structure, function and diversity of the healthy human microbiome. Nature 2012, 486:207-214. 10.1038/nature11234, 3564958, 22699609.
5. Peterson J, Garges S, Giovanni M, McInnes P, Wang L, Schloss JA, Bonazzi V, McEwen JE, Wetterstrand KA, Deal C. The NIH human microbiome project. Genome Res 2009, 19:2317-2323. 2792171, 19819907.
6. Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C, Nielsen T, Pons N, Levenez F, Yamada T. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 2010, 464:59-65. 10.1038/nature08821, 20203603.
7. Moyes DL, Naglik JR. The mycobiome: influencing IBD severity. Cell Host Microbe 2012, 11:551-552. 10.1016/j.chom.2012.05.009, 22704612.
8. Ghannoum MA, Jurevic RJ, Mukherjee PK, Cui F, Sikaroodi M, Naqvi A, Gillevet PM. Characterization of the oral fungal microbiome (mycobiome) in healthy individuals. PLoS Pathog 2010, 6:e1000713. 10.1371/journal.ppat.1000713, 2795202, 20072605.
9. Perfect JR, Casadevall A. Fungal molecular pathogenesis: what can it do and why do we need it?. Molecular Principles of Fungal Pathogenesis 2006, 3-12. Washington DC: ASM Press, Heitman J, Filler SG, Edwards JE, Mitchell AP.
10. Chen Y, Chen Z, Guo R, Chen N, Lu H, Huang S, Wang J, Li L. Correlation between gastrointestinal fungi and varying degrees of chronic hepatitis B virus infection. Diagn Micr Infec Dis 2011, 70:492-498.
11. Nelson A, De Soyza A, Bourke S, Perry J, Cummings S. Assessment of sample handling practices on microbial activity in sputum samples from patients with cystic fibrosis. Lett Appl Microbiol 2010, 51:272-277. 10.1111/j.1472-765X.2010.02891.x, 20629946.
12. Harrison MJ, Twomey KB, McCarthy Y, O'Connell OJ, Alston M, Febrer M, Murphy DM, Ryan RP, Plant BJ. Fungal microbiota in the adult cystic fibrosis (CF) airway: characterization by second-generation sequencing and correlation with standard culture-based methods and clinical phenotype. Ir J Med Sci 2012, 181:S369-S437.
13. Kuehbacher T, Ott SJ, Helwig U, Mimura T, Rizzello F, Kleessen B, Gionchetti P, Blaut M, Campieri M, Fölsch UR, Kamm MA, Schreiber S. Bacterial and fungal microbiota in relation to probiotic therapy (VSL# 3) in pouchitis. Gut 2006, 55:833-841. 10.1136/gut.2005.078303, 1856240, 16401690.
14. Ott SJ, Kühbacher T, Musfeldt M, Rosenstiel P, Hellmig S, Rehman A, Drews O, Weichert W, Timmis KN, Schreiber S. Fungi and inflammatory bowel diseases: alterations of composition and diversity. Scand J Gastroenterol 2008, 43:831-841. 10.1080/00365520801935434, 18584522.
15. Deborah AH, Roberto K. Fungal-bacterial interactions. Molecular Principles of Fungal Pathogenesis 2006, 261-269. Washington DC: ASM Press, Heitman J, Filler SG, Edwards JE, Mitchell AP.
16. Cutler JE, Deepe GS, Klein BS. Advances in combating fungal diseases: vaccines on the threshold. Nat Rev Microbiol 2007, 5:13-28. 10.1038/nrmicro1537, 2214303, 17160002.
17. Marloth RH. An apparatus for the study of matforming fungi in culture solutions. Science 1929, 69:524-525. 10.1126/science.69.1794.524, 17797936.
18. Beck JM, Young VB, Huffnagle GB. The microbiome of the lung. Transl Res 2012, 160:258-266. 10.1016/j.trsl.2012.02.005, 22683412.
19. Delhaes L, Monchy S, Fréalle E, Hubans C, Salleron J, Leroy S, Prevotat A, Wallet F, Wallaert B, Dei-Cas E. The airway microbiota in cystic fibrosis: a complex fungal and bacterial community-implications for therapeutic management. PLoS One 2012, 7:e36313. 10.1371/journal.pone.0036313, 3338676, 22558432.
20. Schoch CL, Seifert KA, Huhndorf S, Robert V, Spouge JL, Levesque CA, Chen W, Bolchacova E, Voigt K, Crous PW. Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for fungi. Proc Natl Acad Sci USA 2012, 109:6241-6246. 10.1073/pnas.1117018109, 3341068, 22454494.
21. Dollive S, Peterfreund GL, Sherrill-Mix S, Bittinger K, Sinha R, Hoffmann C, Nabel C, Hill DA, Artis D, Bachman MA. A tool kit for quantifying eukaryotic rRNA gene sequences from human microbiome samples. Genome Biol 2012, 13:R60. 10.1186/gb-2012-13-7-r60, 22759449.
22. Findley K, Oh J, Yang J, Conlan S, Deming C, Meyer JA, Schoenfeld D, Nomicos E, Park M, , Kong HH, Segre JA. NIH Intramural Sequencing Center Comparative Sequencing Program Topographic diversity of fungal and bacterial communities in human skin. Nature 2013, 498:367-370. 10.1038/nature12171, 23698366, NIH Intramural Sequencing Center Comparative Sequencing Program.
23. Bellemain E, Carlsen T, Brochmann C, Coissac E, Taberlet P, Kauserud H. ITS as an environmental DNA barcode for fungi: an in silico approach reveals potential PCR biases. BMC Microbiol 2010, 10:189-197. 10.1186/1471-2180-10-189, 2909996, 20618939.
24. Nossa CW, Oberdorf WE, Yang L, Aas JA, Paster BJ, DeSantis TZ, Brodie EL, Malamud D, Poles MA, Pei Z. Design of 16S rRNA gene primers for 454 pyrosequencing of the human foregut microbiome. World J Gastroenterol 2010, 16:4135-4144. 10.3748/wjg.v16.i33.4135, 2932916, 20806429.
25. Jumpstart Consortium Human Microbiome Project Data Generation Working Group Evaluation of 16S rDNA-based community profiling for human microbiome research. PLoS One 2012, 7:e39315. 10.1371/journal.pone.0039315, 3374619, 22720093, Jumpstart Consortium Human Microbiome Project Data Generation Working Group.
26. Bartram AK, Lynch MD, Stearns JC, Moreno-Hagelsieb G, Neufeld JD. Generation of multimillion-sequence 16S rRNA gene libraries from complex microbial communities by assembling paired-end illumina reads. Appl Environ Microbiol 2011, 77:3846-3852. 10.1128/AEM.02772-10, 3127616, 21460107.
27. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, Owens SM, Betley J, Fraser L, Bauer M, Gormley N, Gilbert JA, Smith G, Knight R. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J 2012, 6:1621-1624. 10.1038/ismej.2012.8, 3400413, 22402401.
28. Whiteley AS, Jenkins S, Waite I, Kresoje N, Payne H, Mullan B, Allcock R, O'Donnell A. Microbial 16S rRNA ion tag and community metagenome sequencing using the Ion Torrent (PGM) Platform. J Microbiol Methods 2012, 91:80-88. 10.1016/j.mimet.2012.07.008, 22849830.
29. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R. QIIME allows analysis of high-throughput community sequencing data. Nat Methods 2010, 7:335-336. 10.1038/nmeth.f.303, 3156573, 20383131.
30. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 2009, 75:7537-7541. 10.1128/AEM.01541-09, 2786419, 19801464.
31. White JR, Maddox C, White O, Angiuoli SV, Fricke WF. CloVR-ITS: automated internal transcribed spacer amplicon sequence analysis pipeline for the characterization of fungal microbiota. Microbiome 2013, 1:1-11.
32. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 2013, 41:D590-D596. 10.1093/nar/gks1219, 3531112, 23193283.
33. Abarenkov K, Henrik Nilsson R, Larsson KH, Alexander IJ, Eberhardt U, Erland S, Høiland K, Kjøller R, Larsson E, Pennanen T. The UNITE database for molecular identification of fungi-recent updates and future perspectives. New Phytol 2010, 186:281-285. 10.1111/j.1469-8137.2009.03160.x, 20409185.
34. Matsen F, Kodner R, Armbrust EV. pplacer: linear time maximum-likelihood and Bayesian phylogenetic placement of sequences onto a fixed reference tree. BMC Bioinformatics 2010, 11:538. 10.1186/1471-2105-11-538, 3098090, 21034504.
35. Sellart-Altisent M, Torres-Rodríguez JM, Gómez de Ana S, Alvarado-Ramírez E. Nasal fungal microbiota in allergic and healthy subjects. Rev Iberoam Micol 2007, 24:125-130. 10.1016/S1130-1406(07)70027-X, 17604431.
36. Noverr MC, Falkowski NR, McDonald RA, McKenzie AN, Huffnagle GB. Development of allergic airway disease in mice following antibiotic therapy and fungal microbiota increase: role of host genetics, antigen, and interleukin-13. Infect Immun 2005, 73:30-38. 10.1128/IAI.73.1.30-38.2005, 538952, 15618138.
37. Brenchley JM, Price DA, Schacker TW, Asher TE, Silvestri G, Rao S, Kazzaz Z, Bornstein E, Lambotte O, Altmann D, Blazar BR, Rodriguez B, Teixeira-Johnson L, Landay A, Martin JN, Hecht FM, Picker LJ, Lederman MM, Deeks SG, Douek DC. Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat Med 2006, 12:1365-1371.
38. Morris A, Hillenbrand M, Finkelman M, George MP, Singh V, Kessinger C, Lucht L, Busch M, McMahon D, Weinman R. Serum (1→3)-β-D-Glucan levels in HIV-infected individuals are associated with immunosuppression, inflammation, and cardiopulmonary function. J Acquir Immune Defic Syndr 2012, 61:462-468. 10.1097/QAI.0b013e318271799b, 22972021.
39. Darling WM. Co-cultivation of mycobacteria and fungus. Lancet 1976, 2:740.
40. Kerr J. Inhibition of fungal growth by Pseudomonas aeruginosa and Pseudomonas cepacia isolated from patients with cystic fibrosis. J Infect 1994, 28:305-310.
41. Adam B, Baillie GS, Douglas LJ. Mixed species biofilms of Candida albicans and Staphylococcus epidermidis. J Med Microbiol 2002, 51:344-349.
42. Grice EA, Segre JA. The skin microbiome. Nat Rev Microbiol 2011, 9:244-253. 10.1038/nrmicro2537, 3535073, 21407241.
43. Jacobs PH. An overview: antifungal treatment. Fungal Disease: Biology, Immunology, and Diagnosis 1997, 1-5. New York: CRC Press, Jacobs PH, Nall L.
44. Nagata R, Nagano H, Ogishima D, Nakamura Y, Hiruma M, Sugita T. Transmission of the major skin microbiota, Malassezia, from mother to neonate. Pediatr Int 2012, 54:350-355. 10.1111/j.1442-200X.2012.03563.x, 22300401.
45. Jawhara S, Mogensen E, Maggiotto F, Fradin C, Sarazin A, Dubuquoy L, Maes E, Guérardel Y, Janbon G, Poulain D. A murine model of dextran sulfate sodium-induced colitis reveals Candida glabrata virulence and contribution of β-mannosyltransferases. J Biol Chem 2012, 287:11313-11324. 10.1074/jbc.M111.329300, 3322808, 22291009.
46. Netea MG, Gow NA, Munro CA, Bates S, Collins C, Ferwerda G, Hobson RP, Bertram G, Hughes HB, Jansen T, Jacobs L, Buurman ET, Gijzen K, Williams DL, Torensma R, McKinnon A, MacCallum DM, Odds FC, Van der Meer JW, Brown AJ, Kullberg BJ. Immune sensing of Candida albicans requires cooperative recognition of mannans and glucans by lectin and Toll-like receptors. J Clin Invest 2006, 116:1642-1650. 10.1172/JCI27114, 1462942, 16710478.
47. Saijo S, Ikeda S, Yamabe K, Kakuta S, Ishigame H, Akitsu A, Fujikado N, Kusaka T, Kubo S, Chung S-H, Komatsu R, Miura N, Adachi Y, Ohno N, Shibuya K, Yamamoto N, Kawakami K, Yamasaki S, Saito T, Akira S, Iwakura Y. Dectin-2 recognition of α-mannans and induction of Th17 cell differentiation is essential for host defense against Candida albicans. Immunity 2010, 32:681-691. 10.1016/j.immuni.2010.05.001, 20493731.
48. Iliev ID, Funari VA, Taylor KD, Nguyen Q, Reyes CN, Strom SP, Brown J, Becker CA, Fleshner PR, Dubinsky M. Interactions between commensal fungi and the C-type lectin receptor Dectin-1 influence colitis. Science 2012, 336:1314-1317. 10.1126/science.1221789, 3432565, 22674328.
49. van der Velden WJ, Netea MG, de Haan AF, Huls GA, Donnelly JP, Blijlevens N. The role of the mycobiome in human acute graft-versus-host disease. Biol Blood Marrow Transplant 2013, 19:329-332. 10.1016/j.bbmt.2012.11.008, 23160005.
50. Zhang E, Tanaka T, Tajima M, Tsuboi R, Nishikawa A, Sugita T. Characterization of the skin fungal microbiota in patients with atopic dermatitis and in healthy subjects. Microbiol Immunol 2011, 55:625-632. 10.1111/j.1348-0421.2011.00364.x, 21699559.
51. Paulino LC, Tseng CH, Blaser MJ. Analysis of Malassezia microbiota in healthy superficial human skin and in psoriatic lesions by multiplex real-time PCR. FEMS Yeast Res 2008, 8:460-471. 10.1111/j.1567-1364.2008.00359.x, 18294199.
52. McFarland L, Bernasconi P. Saccharomyces boulardii: a review of an innovative biotherapeutic agent. Microb Ecol Health Dis 1993, 6:157-171.
53. Romani L. Immunity to fungal infections. Nat Rev Immunol 2011, 11:275-288. 10.1038/nri2939, 21394104.
54. Cho I, Blaser MJ. The human microbiome: at the interface of health and disease. Nat Rev Genet 2012, 13:260-270. 3418802, 22411464.
55. Ostrosky-Zeichner L, Casadevall A, Galgiani JN, Odds FC, Rex JH. An insight into the antifungal pipeline: selected new molecules and beyond. Nat Rev Drug Discov 2010, 9:719-727. 10.1038/nrd3074, 20725094.
56. Fleuridor R, Zhong Z, Pirofski L. A human IgM monoclonal antibody prolongs survival of mice with lethal cryptococcosis. J Infect Dis 1998, 178:1213-1216. 10.1086/515688, 9806064.
57. Moragues MD, Omaetxebarria MJ, Elguezabal N, Sevilla MJ, Conti S, Polonelli L, Pontón J. A monoclonal antibody directed against a Candida albicans cell wall mannoprotein exerts three anti-C. albicans activities. Infect Immun 2003, 71:5273-5279. 10.1128/IAI.71.9.5273-5279.2003, 187351, 12933874.
58. Nosanchuk JD, Steenbergen JN, Shi L, Deepe GS, Casadevall A. Antibodies to a cell surface histone-like protein protect against Histoplasma capsulatum. J Clin Invest 2003, 112:1164-1175. 213494, 14561701.
59. Chaturvedi AK, Kavishwar A, Keshava GS, Shukla P. Monoclonal immunoglobulin G1 directed against Aspergillus fumigatus cell wall glycoprotein protects against experimental murine aspergillosis. Clin Diagn Lab Immunol 2005, 12:1063-1068. 1235786, 16148172.
60. Korabečná M, Liška V, Fajfrlik K. PrimersITS1, ITS2 andITS4 detect the intraspecies variability in the internal transcribed spacers and 5.8 S rRNA gene region in clinical isolates of fungi. Folia Microbiol 2003, 48:233-238.
61. Esteve-Zarzoso B, Belloch C, Uruburu F, Querol A. Identification of yeasts by RFLP analysis of the 5.8 S rRNA gene and the two ribosomal internal transcribed spacers. Int J Syst Bacteriol 1999, 49:329-337. 10.1099/00207713-49-1-329, 10028278.
62. Scupham AJ, Presley LL, Wei B, Bent E, Griffith N, McPherson M, Zhu F, Oluwadara O, Rao N, Braun J. Abundant and diverse fungal microbiota in the murine intestine. Appl Environ Microbiol 2006, 72:793-801. 10.1128/AEM.72.1.793-801.2006, 1352209, 16391120.
63. Drell T, Lillsaar T, Tummeleht L, Simm J, Aaspõllu A, Väin E, Saarma I, Salumets A, Donders GG, Metsis M. Characterization of the vaginal micro- and mycobiome in asymptomatic reproductive-age Estonian women. PLoS One 2013, 8:e54379. 10.1371/journal.pone.0054379, 3553157, 23372716.
64. Liu L, Li Y, Li S, Hu N, He Y, Pong R, Lin D, Lu L, Law M. Comparison of next-generation sequencing systems. J Biomed Biotechnol 2012, 2012:1-11. 3151496, 21836813.
65. Amend AS, Seifert KA, Samson R, Bruns TD. Indoor fungal composition is geographically patterned and more diverse in temperate zones than in the tropics. Proc Natl Acad Sci USA 2010, 107:13748-13753. 10.1073/pnas.1000454107, 2922287, 20616017.
66. Park HK, Ha M-H, Park S-G, Kim MN, Kim BJ, Kim W. Characterization of the fungal microbiota (mycobiome) in healthy and dandruff-afflicted human scalps. PLoS One 2012, 7:e32847. 10.1371/journal.pone.0032847, 3290624, 22393454.
67. Bosco VL, Birman EG, Cury AE, Paula CR. Yeasts from the oral cavity of children with AIDS: exoenzyme production and antifungal resistance. Pediatr Dent 2003, 17:217-222.
68. Paulino LC, Tseng C-H, Strober BE, Blaser MJ. Molecular analysis of fungal microbiota in samples from healthy human skin and psoriatic lesions. J Clin Microbiol 2006, 44:2933-2941. 10.1128/JCM.00785-06, 1594634, 16891514.
69. Purim K, Bordignon G, Queiroz-Telles F. Fungal infection of the feet in soccer players and non-athlete individuals. Rev Iberoam Micol 2005, 22:34-38. 10.1016/S1130-1406(05)70004-8, 15813681.
70. Santos PM, Melo CM, Martins SA, Chaves Ade A, Sá DSP, Santos RC. Study of ocular fungal microbiota in patients with Hansen's disease and in individuals who deal with them. Arq Bras Oftalmol 2006, 69:915-918. 10.1590/S0004-27492006000600022, 17273688.
71. Thomas JG, Ramage G, Lopez-Ribot JL. Biofilms and implant infections. Microbial Biofilms 2004, 269-293. Washington DC: ASM Press, Ghannoum MA, O'Toole GA.
72. Grimaudo N, Nesbitt W. Coaggregation of Candida albicans with oral Fusobacterium species. Oral Microbiol Immunol 1997, 12:168-173. 10.1111/j.1399-302X.1997.tb00374.x, 9467403.
73. Holmes AR, McNAB R, Jenkinson HF. Candida albicans binding to the oral bacterium Streptococcus gordonii involves multiple adhesin-receptor interactions. Infect Immun 1996, 64:4680-4685. 174431, 8890225.
74. Branting C, Sund M-L, Linder L. The influence of Streptococcus mutans on adhesion of Candida albicans to acrylic surfaces in vitro. Arch Oral Biol 1989, 34:347-353. 10.1016/0003-9969(89)90108-8, 2532001.
75. Wagner RD, Pierson C, Warner T, Dohnalek M, Hilty M, Balish E. Probiotic effects of feeding heat-killed Lactobacillus acidophilus and Lactobacillus casei to Candida albicans-colonized immunodeficient mice. J Food Prot 2000, 63:638-644.
76. Boris S, Barbés C. Role played by Lactobacilli in controlling the population of vaginal pathogens. Microbes Infect 2000, 2:543-546. 10.1016/S1286-4579(00)00313-0, 10865199.